Abstract
Efferent, or downstream, modulation of sensory processing is a common attribute of all sensory systems. However, feedback from the brain directly onto the sensory cells themselves, that is, at the transduction stage, is rare (Robertson 2009). The mechanosensory hair cells of vertebrates are arguably the most sophisticated example of this relationship, and much remains to be learned about efferent modulation of their function under natural conditions. In trying to understand the role of the efferent system, it is instructive to consider its evolution. This chapter discusses the various manifestations of efferent innervation to the hair-cell organs across vertebrates and what we know about its function. From these data, major steps in the evolution of the efferent system can be inferred that in turn allow us to deduce some general rules about efferent function and to define interesting questions for future investigation. The emphasis will be on the auditory system, as Goldberg, Lysakowski and Holt, Chap. 6, already discussed the vestibular efferent system across vertebrates. For orientation on the phylogenetic relationships of the various animal groups discussed here, please refer to the recent review in Manley and Clack (2004).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Amemiya F, Kishida R, Goris RC, Onishi H, Kusunoki T (1985) Primary vestibular projections in the hagfish Eptatretus burgeri. Brain Res 337:73–80
Anadon R, Molist P, Rodriguez-Moldes I, Lopez JM, Quintela I, Cervino MC, Barja P, Gonzalez A (2000) Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula). J Comp Neurol 420:139–170
Art JJ, Fettiplace R, Fuchs PA (1984) Synaptic hyperpolarization and inhibition of turtle cochlear hair cells. J Physiol 356:525–550
Art JJ, Crawford AC, Fettiplace R, Fuchs PA (1985) Efferent modulation of hair cell tuning in the cochlea of the turtle. J Physiol 360:397–421
Arvidsson U, Piehl F, Johnson H, Ulfhake B, Cullheim S, Hökfelt T (1993) The peptidergic motoneurone. Neuroreport 4:849–856
Bagger-Sjöbäck D (1976) The cellular organization and nervous supply of the basilar papilla in the lizard, Calotes versicolor. Cell Tissue Res 165:141–156
Bailey GP, Sewell WF (2000) Calcitonin gene-related peptide suppresses hair cell responses to mechanical stimulation in the Xenopus lateral line organ. J Neurosci 20:5163–5169
Baird IL (1974) Some aspects of the comparative anatomy and evolution of the inner ear in submammalian vertebrates. Brain Behav Evol 10:11–36
Barbas-Henry HA, Lohman AHM (1988) Primary projections and efferent cells of the VIIIth cranial nerve in the monitor lizard, Varanus exanthematicus. J Comp Neurol 277:234–249
Bell C (1981) Central distribution of octavolateral afferents and efferents in a teleost (Mormyridae). J Comp Neurol 195:391–414
Birinyi A, Straka H, Matesz C, Dieringer N (2001) Location of dye-coupled second order and of efferent vestibular neurons labeled from individual semicircular canal or otolith organs in the frog. Brain Res 921:44–59
Bleckmann H, Niemann U, Fritzsch B (1991) Peripheral and central aspects of the acoustic and lateral line system of a bottom dwelling catfish, Ancistrus sp. J Comp Neurol 314:452–466
Bodznick D, Northcutt RG (1981) Electro reception in lampreys Lampetra tridentata: evidence that the earliest vertebrates were electro receptive. Science 212:465–467
Brantley RK, Bass AH (1988) Cholinergic neurons in the brain of a teleost fish (Porichthys notatus) located with a monoclonal antibody to choline acetyltransferase. J Comp Neurol 275:87–105
Braun CB, Northcutt RG (1997) The lateral line system of hagfishes (Craniata: Myxinoidea). Acta Zool 78:247–268
Bricaud O, Chaar V, Dambly-Chaudiere C, Ghysen A (2001) Early efferent innervation of the zebrafish lateral line. J Comp Neurol 434:253–261
Burgess BJ, Adams JC, Nadol JB Jr (1997) Morphologic evidence for innervation of Deiters’ and Hensen’s cells in the guinea pig. Hear Res 108:74–82
Burighel P, Lane NJ, Fabio G, Stefano T, Zaniolo G, Daniela M, Carnevali C, Manni L (2003) Novel, secondary sensory cell organ in ascidians: in search of the ancestor of the vertebrate lateral line. J Comp Neurol 461:236–249
Caicci F, Burighel P, Manni L (2007) Hair cells in an ascidian (Tunicata) and their evolution in chordates. Hear Res 231:63–72
Caston J, Bricout-Berthout A (1982) Responses of afferent and efferent neurons to visual inputs in the vestibular nerve of the frog. Brain Res 240:141–145
Caston J, Roussel H (1984) Curare and the efferent vestibular system. Acta Otolaryngol 97:19–26
Chandler JP (1984) Light and electron microscopic studies of the basilar papilla in the duck. Anas platyrhynchos. I. The hatchling. J Comp Neurol 222:506–522
Chang JSY, Popper AN, Saidel WM (1992) Heterogeneity of sensory hair cells in a fish ear. J Comp Neurol 324:621–640
Changeaux J-P, Duclert A, Sekine S (1992) Calcitonin gene-related peptides and neuromuscular interactions. Ann N Y Acad Sci 657:361–378
Chiappe ME, Kozlov AS, Hudspeth AJ (2007) The structural and functional differentiation of hair cells in a lizard’s basilar papilla suggests an operational principle of amniote cochleas. J Neurosci 27:11978–11985
Claas B, Münz H (1980) Bonyfish lateral line efferent neurons identified by retrograde axonal transport of horseradish peroxidase (HRP). Brain Res 193:249–253
Claas B, Fritzsch B, Münz H (1981) Common efferents to lateral line and labyrinthine hair cells in aquatic vertebrates. Neurosci Lett 27:231–235
Clemente D, Porteros A, Weuaga E, Alonso JR, Arenzana FJ, Aijón J, Arévalo R (2004) Cholinergic elements in the zebrafish central nervous system: histochemical and immunohistochemical analysis. J Comp Neurol 474:75–107
Code RA (1995) Efferent neurons to the macula lagena in the embryonic chick. Hear Res 82:26–30
Code RA (1996) Chick auditory terminals contain dynorphin-like immunoreactivity. Neuroreport 7:2917–2920
Code RA (1997) The avian cochlear efferent system. Poultry Avian Biol Rev 8:1–8
Code RA, Carr CE (1994) Choline acetyltransferase-immunoreactive cochlear efferent neurons in the chick auditory brainstem. J Comp Neurol 340:161–173
Code RA, Carr CE (1995) Enkephalin-like immunoreactivity in the chick brainstem: possible relation to the cochlear efferent system. Hear Res 87:69–83
Code RA, Darr MS, Carr CE (1996) Chick cochlear efferent neurons are not immunoreactive for calcitonin gene-related peptide. Hear Res 97:127–135
Coffin AB, Kelley M, Manley GA, Popper AN (2004) Evolution of sensory hair cells. In: Manley GA, Popper A, Fay RR (eds) Evolution of the vertebrate auditory system. Springer, New York, pp 55–94
Cole KS, Gummer AW (1990) A double-label study of efferent projections to the cochlea of the chicken, Gallus domesticus. Exp Brain Res 82:585–588
Corwin JT (1977) Morphology of the macula neglecta in sharks of the genus Carcharhinus. J Morphol 152:341–362
Cotanche DA, Henson MM, Henson OW Jr (1992) Contractile proteins in the hyaline cells of the chicken cochlea. J Comp Neurol 324:353–364
Dailey SH, Wackym PA, Brichta AM, Gannon PJ, Popper P (2000) Topographic distribution of nicotinic acetylcholine receptors in the cristae of a turtle. Hear Res 141:51–56
Daniels MP (1997) Intercellular communication that mediates formation of the neuromuscular junction. Mol Neurobiol 14:143–170
Danielson PD, Zottoli SJ, Corrodi JG, Rhodes KJ, Mufson EJ (1988) Localization of choline acetyltransferase to somata of posterior lateral line efferents in the goldfish. Brain Res 448:158–161
Drenckhahn D, Merte C, von Düring M, Smolders J, Klinke R (1991) Actin, myosin and alpha-actinin containing filament bundles in hyaline cells of the caiman cochlea. Hear Res 54:29–38
Drescher DG, Ramakrishnan NA, Drescher MJ, Chun W, Wang X, Myers SF, Green GE, Sadrazodi K et al (2004) Cloning and characterization of alpha 9 subunits of the nicotinic acetylcholine receptor expressed by saccular hair cells of the rainbow trout (Oncorhynchus mykiss). Neuroscience 127:737–752
Dulon D, Blanchet C, Laffon E (1994) Photo-released intracellular Ca2+ evolkes reversible mechanical responses in supporting cells of the guinea-pig organ of Corti. Biochem Biophys Res Commun 201:1263–1269
Edds-Walton PL, Fay RR, Highstein SM (1999) Dendritic arbors and central projections of physiologically characterized auditory fibers from the saccule of the toadfish, Opsanus tau. J Comp Neurol 411:212–238
Firbas W, Müller G (1983) The efferent innervation of the avian cochlea. Hear Res 10:109–116
Fischer FP (1992) Quantitative analysis of the innervation of the chicken basilar papilla. Hear Res 61:167–178
Fischer FP (1994a) General pattern and morphological specializations of the avian cochlea. Scanning Microsc 8:351–364
Fischer FP (1994b) Quantitative TEM analysis of the barn owl basilar papilla. Hear Res 73:1–15
Fischer FP (1998) Hair-cell morphology and innervation in the basilar papilla of the emu (Dromaius novaehollandiae). Hear Res 121:112–124
Fischer FP, Miltz C, Singer I, Manley GA (1992) Morphological gradients in the starling basilar papilla. J Morphol 213:225–240
Fischer FP, Eisensamer B, Manley GA (1994) Cochlear and lagenar ganglia of the chicken. J Morphol 220:71–83
Flock A (1965) The ultrastructure and microphonic potential of the lateral line canal organ. Acta Otolaryngol 59(suppl 199):7–90
Flock A, Flock B (1966) Ultrastructure of the amphibian papilla in the bullfrog. J Acoust Soc Am 40:1262
Franchini LF, Elgoyhen AB (2006) Adaptive evolution in mammalian proteins involved in cochlear outer hair cell electromotility. Mol Phylogenet Evol 41:622–635
Frishkopf LS, Flock A (1974) Ultrastructure of the basilar papilla, an auditory organ in the bullfrog. Acta Otolaryngol (Stockh) 77:176–184
Fritzsch B (1981) Efferent neurons to the labyrinth of Salamandra salamandra as revealed by retrograde transport of horseradish peroxydase. Neurosci Lett 26:191–196
Fritzsch B (1997) On the role played by ontogenetic remodeling and functional transformation in the evolution of terrestrial hearing. Brain Behav Evol 50:38–49
Fritzsch B (1999) Ontogenetic and evolutionary evidence for the motoneuron nature of vestibular and cochlear efferents. In: Berlin CI (ed) The efferent auditory system: basic science and clinical applications. Singular Publishing, San Diego, pp 31–59
Fritzsch B, Crapon de Caprona D (1984) The origin of centrifugal inner ear fibers of gymnophions (amphibia). A horseradish peroxidase study. Neurosci Lett 46:131–136
Fritzsch B, Wahnschaffe U (1987) Electron microscopical evidence for common inner ear and lateral line efferents in urodeles. Neurosci Lett 81:48–52
Fritzsch B, Dubuc R, Otha Y, Grillner S (1989) Efferents to the labyrinth of the river lamprey (Lampetra fluviatilis) as revealed with retrograde tracing techniques. Neurosci Lett 96:241–246
Fuchs PA, Murrow BW (1992) Cholinergic inhibition of short (outer) hair cells of the chick’s cochlea. J Neurosci 12:800–809
Fuchs P, Zidanic M, Michaels R, Yuhas W, Jiang GJ (1998) Ion channels and synaptic function in chick cochlear hair cells. In: Palmer AR, Rees A, Summerfield AQ, Meddis R (eds) Psychophysical and psychological advances in hearing. Whurr Publishers, London, pp 97–104
Gans C, Wever EG (1976) Ear and hearing in Sphenodon punctatus. Proc Natl Acad Sci U S A 73:4244–4246
Gleich O, Manley GA (2000) The hearing organ of birds and crocodilia. In: Dooling RJ, Fay RR, Popper AN (eds) Comparative hearing: birds and reptiles. Springer, New York, pp 70–138
Goldberg JM, Brichta AM, Wackym PA (2000) Efferent vestibular system: anatomy, physiology, and neurochemistry. In: Beitz AJ, Anderson JH (eds) Neurochemistry of the vestibular system. CRC Press, Boca Raton, pp 61–94
Gonzalez A, Meredith GE, Roberts BL (1993) Choline acetyltransferase immunoreactive neurons innervating labyrinthine and lateral line sense organs in amphibians. J Comp Neurol 332:258–268
Guinan JJJ (1996) Physiology of olivocochlear efferents. In: Dallos P, Popper AN, Fay RR (eds) The cochlea. Springer, New York, pp 435–502
Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox A et al (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768
Hama K (1965) Some observations on the fine structure of the lateral line organ of the Japanese sea eel Lyncozymba nystromi. J Cell Biol 24:193–210
Hama K (1969) A study on the fine structure of the saccular macula of the gold fish. Z Zellforsch 94:155–171
Hartmann R, Klinke R (1980) Efferent activity in the goldfish vestibular nerve and its influence on afferent activity. Pflügers Arch 388:123–128
Hellmann B, Fritzsch B (1996) Neuroanatomical and histochemical evidence for the presence of common lateral line and inner ear efferents and of efferents to the basilar papilla in a frog, Xenopus laevis. Brain Behav Evol 47:185–194
Hiel H, Luebke AE, Fuchs PA (2000) Cloning and expression of the alpha 9 nicotinic acetylcholine receptor subunit in cochlear hair cells of the chick. Brain Res 858:215–225
Highstein SM, Baker R (1986) Organsization of the efferent vestibular nuclei and nerves of the toadfish, Opsanus tau. J Comp Neurol 243:309–325
Hirokawa N (1978) The ultrastructure of the basilar papilla of the chick. J Comp Neurol 181:361–374
Hoshino T (1975) An electron microscopic study of the otolithic maculae of the lamprey (Entosphenus japonicus). Acta Otolaryngol 80:43–53
Housley GD, Ashmore JF (1991) Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc R Soc Lond B 244:161–167
Jande SS (1966) Fine structure of lateral-line organs of frog tadpoles. J Ultrastruct Res 15:496–509
Janvier P (2008) Early jawless vertebrates and cyclostome origins. Zool Sci 25:1045–1056
Jones TA, Jones SM, Paggett KC (2001) Primordial rhythmic bursting in embryonic cochlear ganglion cells. J Neurosci 21:8129–8135
Jones TA, Leake PA, Snyder RL, Stakhovskaya O, Bonham B (2007) Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats. J Neurophysiol 98:1898–1908
Kaiser A (1993) Das efferente Bündel des Hörorgans beim Huhn – Ursprung, Projektionen und Physiologie [Dr.rer.nat.]. Garching, Technische Universität München, p 167
Kaiser A, Manley GA (1994) Physiology of single putative cochlear efferents in the chicken. J Neurophysiol 72:2966–2979
Kaiser A, Manley GA (1996) Brainstem connections of the macula lagenae in the chicken. J Comp Neurol 374:108–117
Keppler C, Schermuly L, Klinke R (1994) The course and morphology of efferent nerve fibres in the papilla basilaris of the pigeon (Columba livia). Hear Res 74:259–264
Khan KM, Hatfield JS, Drescher MJ, Drescher DG (1991) The histochemical localization of acetylcholinesterase in the rainbow trout saccular macula by electron microscopy. Neurosci Lett 131:109–112
Khan KM, Drescher MJ, Hatfield JS, Khan A-M, Drescher DG (2002) Muscarinic receptor subtypes are differentially distributed in the rat cochlea. Neuroscience 111:291–302
Kirk EC, Smith DW (2003) Protection from acoustic trauma is not a primary function of the medial olivocochlear efferent system. J Assoc Res Otolaryngol 4:445–465
Kishida R, Goris RC, Nishizawa H, Koyama H, Kadota T, Amemiya F (1987) Primary neurons of the lateral line nerves and their central projections in hagfishes. J Comp Neurol 264:303–310
Köppl C (2001) Efferent axons in the avian auditory nerve. Eur J Neurosci 13:1889–1901
Köppl C (2007) Spontaneous generation in early sensory development. Invited Focus on: Spontaneous discharge patterns in cochlear spiral ganglion cells prior to the onset of hearing in cats. J Neurophysiol 98:1843–1844
Köppl C, Manley GA (1992) Functional consequences of morphological trends in the evolution of lizard hearing organs. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 489–510
Köppl C, Yates GK (1999) Coding of sound pressure level in the barn owl’s auditory nerve. J Neurosci 19:9674–9686
Köppl C, Gleich O, Manley GA (1993) An auditory fovea in the barn owl cochlea. J Comp Physiol A 171:695–704
Köppl C, Gleich O, Schwabedissen G, Siegl E, Manley GA (1998) Fine structure of the basilar papilla of the emu: implications for the evolution of avian hair-cell types. Hear Res 126:99–112
Koyama H, Kishida R, Goris RC, Kusunoki TT (1989) Afferent and efferent projections of the VIIIth cranial nerve in the lamprey, Lampetra japonica. J Comp Neurol 280:663–671
Koyama H, Kishida R, Goris RC, Kusunoki T (1990) Organisation of the primary projections of the lateral line in nerves in the lamprey Lampetra japonica. J Comp Neurol 295:277–289
Le Prell CG (2007) Role for the lateral olivocochlear neurons in auditory function. Focus on: Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury. J Neurophysiol 97:963–965
Le Prell CG, Dolan DF, Halsey K, Hughes L (2007) Chronic intra-cochlear delivery of CGRP, a lateral olivocochlear transmitter, enhances auditory nerve activity. Assoc Res Otolaryngol Abstr 30:120
Lewis ER, Narins PM (1999) The acoustic periphery of amphibians: anatomy and physiology. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 101–154
Liberman MC, Kujawa SG (1999) The olivocochlear system and protection from acoustic injury: Acute and chronic effects. In: Berlin CI (ed) The efferent auditory system: basic science and clinical applications. Singular Publishing, San Diego, pp 1–29
Lippe WR, Zirpel L, Stone JS (2002) Muscarinic receptors modulate intracellular Ca2+ concentration in hyaline cells of the chicken basilar papilla. J Comp Physiol A 188:381–395
Lopez I, Meza G (1988) Neurochemical evidence for afferent GABAergic and efferent cholinergic neurotransmission in the frog vestibule. Neuroscience 25:13–18
Lowenstein O, Thornhill RA (1970) The labyrinth of Myxine: anatomy, ultrastructure and electrophysiology. Proc R Soc B Biol Sci 176:21–42
Lowenstein O, Osborne MP, Thornhill RA (1968) The anatomy and ultrastructure of the labyrinth of the lamprey (Lampetra fluviatilis L.). Proc R Soc B Biol Sci 170:113–134
Lustig LR, Hiel H, Fuchs PA (1999) Vestibular hair cells of the chick express the nicotinic acetylcholine receptor subunit α9. J Vestib Res 9:359–367
Lysakowski A, Goldberg JM (2004) Morphophysiology of the vestibular periphery. In: Highstein SM, Fay RR, Popper AN (eds) The vestibular system. Springer, New York, pp 57–152
Maison SF, Emeson RB, Adams JC, Luebke AE, Liberman MC (2003) Loss of alpha CGRP reduces sound-evoked activity in the cochlear nerve. J Neurophysiol 90:2941–2949
Manley GA (1990) Peripheral hearing mechanisms in reptiles and birds. Springer, Berlin, p 288
Manley GA (2001) Evidence for an active process and a cochlear amplifier in nonmammals. J Neurophysiol 86:541–549
Manley GA (2004) The lizard basilar papilla and its evolution. In: Manley GA, Popper A, Fay RR (eds) Evolution of the vertebrate auditory system. Springer, New York, pp 200–223
Manley GA, Clack JA (2004) An outline of the evolution of vertebrate hearing organs. In: Manley GA, Popper A, Fay RR (eds) Evolution of the vertebrate auditory system. Springer, New York, pp 1–26
Manley GA, Köppl C (1998) Phylogenetic development of the cochlea and its innervation. Curr Opin Neurobiol 8:468–474
Manley GA, Ladher R (2008) Phylogeny and evolution of ciliated mechanoreceptor cells. In: Dallos P, Oertel D (eds) Audition. Academic Press, San Diego, pp 1–34
Manley GA, Gleich O, Kaiser A, Brix J (1989) Functional differentiation of sensory cells in the avian auditory periphery. J Comp Physiol A 164:289–296
Manley GA, Taschenberger G, Oeckinghaus H (1999) Influence of contralateral acoustic stimulation on distortion-product and spontaneous otoacoustic emissions in the barn owl. Hear Res 138:1–12
Manni L, Caicci F, Gasparini F, Zaniolo G, Burighel P (2004) Hair cells in ascidians and the evolution of lateral line placodes. Evol Dev 6:379–381
Manni L, Mackie GO, Caicci F, Zaniolo G, Burighel P (2006) Coronal organ of ascidians and the evolutionary significance of secondary sensory cells in chordates. J Comp Neurol 495:363–373
Martin P (2008) Active hair-bundle motility of the hair cells of vestibular and auditory organs. In: Manley GA, Fay RR, Popper AN (eds) Active processes and otoacoustic emissions in hearing. Springer, New York, pp 93–144
Martínez-García F, Novejarque A, Landete JM, Moncho-Bogani J, Lanuza E (2002) Distribution of calcitonin gene-related peptide-like immunoreactivity in the brain of the lizard Podarcis hispanica. J Comp Neurol 447:99–113
Matsunobu T, Chung JW, Schacht J (2001) Acetylcholine-evoked calcium increases in Deiters’ cells of the guinea pig cochlea suggest alpha 9-like receptors. J Neurosci Res 63:252–256
McWilliam PN, Maqbool A, Batten TFC, Kaye JC (1995) Influence of peripheral targets on the expression of calcitonin gene-related peptide immunoreactivity in rat cranial motoneurones. J Neurobiol 28:506–514
Medina L, Reiner A (1994) Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342:497–537
Medina L, Smeets WJAJ, Hoogland PV, Puelles L (1993) Distribution of choline acetyltransferase immunoreactivity in the brain of the lizard Gallotia galloti. J Comp Neurol 331:261–285
Meredith GE, Roberts BL (1986) Central organization of the efferent supply to the labyrinthine and lateral line receptors of the dogfish. Neuroscience 17:225–233
Meredith GE, Roberts BL (1987) Distribution and morphological characteristics of efferent neurons innervating end organs in the ear and lateral line of the European eel. J Comp Neurol 265:494–506
Metcalfe WK, Kimmel CB, Schabtach E (1985) Anatomy of the posterior lateral line system in young larvae of the zebrafish. J Comp Neurol 233:377–389
Micevych PE, Kruger L (1992) The status of calcitonin gene-related peptide as an effector peptide. Ann N Y Acad Sci 657:379–396
Miller MR, Beck J (1988) Auditory hair cell innervational patterns in lizards. J Comp Neurol 271:604–628
Miller MR, Beck J (1990) Further serial transmission electron microscopy studies of auditory hair cell innervation in lizards and in a snake. Am J Anat 188:175–184
Molist P, Rodriguez-Moldes I, Batten TFC, Anadon R (1995) Distribution of calcitonin gene-related peptide-like immunoreactivity in the brain of the small-spotted dogfish, Scyliorhinus canicula L. J Comp Neurol 352:335–350
Mueller T, Vernier P, Wullimann MF (2004) The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Res 1011:156–169
Mulroy MJ (1986) Patterns of afferent synaptic contacts in the alligator lizard’s cochlea. J Comp Neurol 248:263–271
Mulroy MJ, Oblak TG (1985) Cochlear nerve of the alligator lizard. J Comp Neurol 233:463–472
Nakajima Y, Wang DW (1974) Morphology of afferent and efferent synapses in hearing organ of the goldfish. J Comp Neurol 156:403–416
New JG, Northcutt RG (1984) Central projections of the lateral line nerves in the shovelnose sturgeon. J Comp Neurol 225:129–140
New JG, Singh S (1994) Central topography of anterior lateral line nerve projections in the channel catfish, Ictalurus punctatus. Brain Behav Evol 43:34–50
Northcutt RG (2005) The new head hypothesis revisited. J Exp Zool B 304B:274–297
Oesterle EC, Cunningham DE, Rubel EW (1992) Ultrastructure of hyaline, border, and vacuole cells in chick inner ear. J Comp Neurol 318:64–82
Ofsie MS, Cotanche DA (1996) Distribution of nerve fibers in the basilar papilla of normal and sound-damaged chick cochleae. J Comp Neurol 370:281–294
Ofsie MS, Hennig AK, Messana EP, Cotanche DA (1997) Sound damage and gentamicin treatment produce different patterns of damage to the efferent innervation of the chick cochlea. Hear Res 113:207–223
Ohno K, Takeda N, Yamano M, Matsunaga T, Tohyama M (1991) Coexistence of acetylcholine and calcitonin gene-related peptide in the vestibular efferent neurons in the rat. Brain Res 566:103–107
Okoruwa OE, Weston MD, Sanjeevi DC, Millemon AR, Fritzsch B, Hallworth R, Beisel KW (2008) Evolutionary insights into the unique electromotility motor of mammalian outer hair cells. Evol Dev 10:300–315
Patterson WC (1966) Hearing in the turtle. J Audit Res 6:453–464
Pellegrini M, Ceccotti F, Magherini P (1985) The efferent vestibular neurons in the toad (Bufo bufo L.): their location and morphology. A horseradish peroxidase study. Brain Res 344:1–8
Pombal MA, Marin O, Gonzalez A (2001) Distribution of choline acetyltransferase-immunoreactive structures in the lamprey brain. J Comp Neurol 431:105–126
Popper AN, Fay RR (1999) The auditory periphery in fishes. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, New York, pp 43–100
Popper AN, Hoxter B (1987) Sensory and nonsensory ciliated cells in the ear of the sea lamprey, Petromyzon marinus. Brain Behav Evol 30:43–61
Popper AN, Saidel WM (1990) Variations in receptor cell innervation in the saccule of a teleost fish ear. Hear Res 46:211–228
Powers SA, Reiner A (1993) The distribution of cholinergic neurons in the central nervous system of turtles. Brain Behav Evol 41:326–345
Prigioni I, Valli P, Casella C (1983) Peripheral organization of the vestibular efferent system in the frog: an electrophysiological study. Brain Res 269:83–90
Pujol R, Lavigne-Rebillard M, Lenoir M (1998) Development of sensory and neural structures in the mammalian cochlea. In: Rubel EW, Popper AN, Fay RR (eds) Development of the auditory system. Springer, New York, pp 146–192
Puzdrowski RL (1989) Peripheral distribution and central projections of the lateral-line nerves in goldfish, Carassius auratus. Brain Behav Evol 34:110–131
Raabe T (2004) Ursprung der cochleären Efferenzen im Hirnstamm der Schleiereule (Tyto alba) [Dr.rer.nat.]. Freising-Weihenstephan, Technische Universität München, p 101
Raabe T, Köppl C (2003a) Bilaterally-projecting efferent neurones to the basilar papilla in the barn owl and the chicken. Brain Res 986:124–131
Raabe T, Köppl C (2003b) Cochlear efferents in different avian species – a way to distinguish between auditory and vestibular? In: Abstracts 26th midwinter research meeting ARO:92
Rajan R (2000) Centrifugal pathways protect hearing sensitivity at the cochlea in noisy environments that exacerbate the damage induced by loud sound. J Neurosci 20:6684–6693
Raji-Kubba J, Micevych PE, Simmons DD (2002) The superior olivary complex of the hamster has multiple periods of cholinergic neuron development. J Chem Neuroanat 24:75–93
Rebillard M, Pujol R (1983) Innervation of the chicken basilar papilla during its development. Acta Otolaryngol (Stockh) 96:379–388
Robbins RG, Bauknight MS, Honrubia V (1967) Anatomical distribution of efferent fibers in the VIIIth cranial nerve of the bullfrog (Rana catesbeiana). Acta Otolaryngol 64:436–448
Roberts BL, Meredith GE (1992) The efferent innervation of the ear: variations on an enigma. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 185–210
Roberts BL, Russell IJ (1972) The activity of lateral-line efferent neurones in stationary and swimming dog-fish. J Exp Biol 57:435–448
Roberts BL, Maslam S, Los I, Van DJB (1994) Coexistence of calcitonin gene-related peptide and choline acetyltransferase in EEL efferent neurons. Hear Res 74:231–237
Robertson D (2009) Centrifugal control in mammalian hearing. Clin Exp Pharmacol Physiol 36:603–611
Robertson D, Mulders WHAM (2000) Distribution and possible functional roles of some neuroactive peptides in the mammalian superior olivary complex. Microsc Res Tech 51:307–317
Ronan MC, Bodznick D (1986) End buds non-ampullary electroreceptors in adult lampreys. J Comp Physiol A 158:9–16
Ronan M, Northcutt RG (1987) Primary projections of the lateral line nerves in adult lampreys. Brain Behav Evol 30:62–81
Rossi ML, Prigioni I, Valli P, Casella C (1980) Activation of the efferent system in the isolated frog labyrinth: effects on the afferent EPSPs and spike discharge recorded from single fibres of the posterior nerve. Brain Res 185:125–137
Ruel J, Wang J, Rebillard G, Eybalin M, Lloyd R, Pujol R, Puel JL (2007) Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear Res 227:19–27
Russell IJ (1971a) The pharmacology of efferent synapses in the lateral-line system of Xenopus laevis. J Exp Biol 54:643–658
Russell IJ (1971b) The role of the lateral-line efferent system in Xenopus laevis. J Exp Biol 54:621–641
Russell IJ (1976) Central inhibition of lateral line input in the medulla of the goldfish by neurons which control active body movements. J Comp Physiol 111:335–358
Russell IJ, Lukashkin AN (2008) Cellular and molecular mechanisms in the efferent control of cochlear nonlinearities. In: Manley GA, Fay RR, Popper AN (eds) Active processes and otoacoustic emissions in hearing. Springer, New York, pp 343–380
Russell IJ, Roberts BL (1972) Inhibition of spontaneous lateral-line activity by efferent nerve stimulation. J Exp Biol 57:77–82
Russell IJ, Roberts BL (1974) Active reduction of lateral-line sensitivity in swimming dogfish. J Comp Physiol 94:7–15
Sapede D, Rossel M, Dambly-Chaudiere C, Ghysen A (2005) Role of SDF1 chemokine in the development of lateral line efferent and facial motor neurons. Proc Natl Acad Sci USA 102:1714–1718
Schellart NAM, Prins M, Kroese ABA (1992) The pattern of trunk lateral line afferents and efferents in the rainbow trout (Salmo gairdneri). Brain Behav Evol 39:371–380
Schmidt RS (1963) Frog labyrinthine efferent impulses. Acta Otolaryngol 56:51–64
Schmidt R (1965) Amphibian acoustico-lateralis efferents. J Cell Comp Physiol 65:155–162
Schucker FA (1972) A preliminary report on light and electron microscopic studies of the basilar papilla in the toad, Xenopus laevis. Anat Rec 172:400
Schwarz IE, Schwarz DWF, Frederickson JM, Landolt JP (1981) Efferent vestibular neurons: A study employing retrograde tracer methods in the pigeon (Columba livia). J Comp Neurol 196:1–12
Schwarz DWF, Schwarz IE, Dezsoe A (1992) Cochlear efferent neurons projecting to both ears in the chicken, Gallus domesticus. Hear Res 60:110–114
Sewell WF, Starr PA (1991) Effects of calcitonin gene-related peptide and efferent nerve stimulation on afferent transmission in the lateral line organ. J Neurophysiol 65:1158–1169
Shigemoto T, Ohmori H (1990) Muscarinic agonists and ATP increase the intracellular Ca2+ concentration in chick cochlear hair cells. J Physiol 420:127–148
Simmons DD, Bertolotto C, Leong M (1995) Synaptic ultrastructure within the amphibian papilla of Rana pipiens pipiens: rostrocaudal differences. Audit Neurosci 1:183–193
Slepecky NB (1996) Structure of the mammalian cochlea. In: Dallos P, Popper AN, Fay RR (eds) The cochlea. Springer, New York, pp 44–129
Smotherman M, Narins P (2004) Evolution of the amphibian ear. In: Manley GA, Popper A, Fay RR (eds) Evolution of the vertebrate auditory system. Springer, New York, pp 164–199
Sneary MG (1988) Auditory receptor of the red-eared turtle: II. Afferent and efferent synapses and innervation patterns. J Comp Neurol 276:588–606
Song J, Northcutt RG (1991) The primary projections of the lateral-line nerves of the Florida gar, Lepisosteus platyrhincus. Brain Behav Evol 37:38–63
Strutz J (1981) The origin of centrifugal fibers to the inner ear in Caiman crocodilus. A horseradish peroxidase study. Neurosci Lett 27:95–100
Strutz J (1982) The origin of efferent fibers to the inner ear in a turtle (Terrapene ornata). A horseradish peroxidase study. Brain Res 244:165–168
Strutz J, Schmidt CL (1982) Acoustic and vestibular efferent neurons in the chicken (Gallus domesticus). Acta Otolaryngol (Stockh) 94:45–51
Strutz J, Schmidt CL, Stürmer C (1980) Origin of efferent fibers of the vestibular apparatus in goldfish. A horseradish peroxidase study. Neurosci Lett 18:5–9
Strutz J, Bielenberg K, Spatz WB (1982) Location of efferent neurons to the labyrinth of the green tree frog (Hyla cinerea). Arch Otorhinolaryngol 234:245–251
Sugai T, Yano J, Sugitani M, Ooyama H (1992) Actions of cholinergic agonists and antagonists on the efferent synapse in the frog sacculus. Hear Res 61:56–64
Sugihara I (2001) Efferent innervation in the goldfish saccule examined by acetylcholinesterase histochemistry. Hear Res 153:91–99
Taberner AM, Liberman MC (2005) Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93:557–569
Takami K, Kawai Y, Shiosaka S, Lee Y, Girgis S, Hillyard CJ, MacIntyre I, Emson PC et al (1985) Immunohistochemicai evidence for the coexistence of calcitonin gene-related peptide- and choline acetyltransferase-like immunoreactivity in neurons of the rat hypoglossal, facial and ambiguus nuclei. Brain Res 328:386–389
Takasaka T, Smith CA (1971) The structure and innervation of the pigeon’s basilar papilla. J Ultrastruct Res 35:20–65
Tanaka K, Smith CA (1978) Structure of the chicken’s inner ear: SEM and TEM study. Am J Anat 153:251–272
Teresi PC (1985) Hair cell innervation patterns in the papilla basilaris of the fence lizard Sceloporus occidentalis. Dissertation, University of California, San Francisco
Tomchik SM, Lu ZM (2005) Octavolateral projections and organization in the medulla of a teleost fish, the sleeper goby (Dormitator latifrons). J Comp Neurol 481:96–117
Tomchik SM, Lu ZM (2006a) Auditory physiology and anatomy of octavolateral efferent neurons in a teleost fish. J Comp Physiol A 192:51–67
Tomchik SM, Lu ZM (2006b) Modulation of auditory signal-to-noise ratios by efferent stimulation. J Neurophysiol 95:3562–3570
Tricas TC, Highstein SM (1991) Action of the octavolateralis efferent system upon the lateral line of free-swimming toadfish, Opsanus tau. J Comp Physiol A 169:25–37
Tritsch NX, Yi EY, Gale JE, Glowatzki E, Bergles DE (2007) The origin of spontaneous activity in the developing auditory system. Nature 450:50–56
Vetter DE, Adams JC, Mugnaini E (1991) Chemically distinct rat olivocochlear neurons. Synapse 7:21–43
Vidal N, Hedges SB (2009) The molecular evolutionary tree of lizards, snakes, and amphisbaenians. C R Biol 332:129–139
von Düring M, Karduck A, Richter H-G (1974) The fine structure of the inner ear in Caiman crocodilus. Z Anat Entwickl Gesch 145:41–65
Wagner T, Schwartz E (1996) Efferent neurons of the lateral line system and their innervation of lateral line branches in a euteleost and an osteoglossomorph. Anat Embryol 194:271–278
Walsh EJ, McGee J (1997) Does activity in the olivochochlear bundle affect development of the auditory periphery? In: Lewis ER, Long G, Lyon RF, Narins PM, Steele CR, Hecht-Poinar E (eds) Diversity in auditory mechanics. World Scientific, Singapore, pp 376–385
Walsh EJ, McGee J, McFadden SL, Liberman MC (1998) Long-term effects of sectioning the olivocochlear bundle in neonatal cats. J Neurosci 18:3859–3869
Warr WB (1992) Organization of olicocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 410–448
Weeg MS, Land BR, Bass AH (2005) Vocal pathways modulate efferent neurons to the inner ear and lateral line. J Neurosci 25:5967–5974
Wegner N (1982) A qualitative and quantitative study of a sensory epithelium in the inner ear of a fish (Colisa labiosa; Anabnatidae). Acta Zool 63:133–146
Wever EG (1978) The reptile ear. Princeton University Press, Princeton
White J (1986) Morphological and fine structural features of the basilar papilla in ambystomatid salamanders (Amphibia; Caudata). J Morphol 187:181–199
Whitehead MC, Morest DK (1981) Dual populations of efferent and afferent cochlear axons in the chicken. Neuroscience 6:2351–2365
Whitehead MC, Morest DK (1985) The growth of cochlear fibers and the formation of their synaptic endings in the avian inner ear: a study with the electron microscope. Neuroscience 14:277–300
Wibowo E, Brockhausen J, Köppl C (2008) Efferent innervation is present to both low- and high-frequency regions of the auditory basilar papilla of lizards. In: 38th annual meeting of the society for neuroscience. Society for Neuroscience, Washington, DC, Program No. 259.251
Wibowo E, Brockhausen J, Köppl C (2009) Efferent innervation to the auditory basilar papilla of scincid lizards. J Comp Neurol 516:74–85
Wicht H, Northcutt RG (1995) Ontogeny of the head of the Pacific hagfish (Eptatretus stouti, Myxinoidea): Development of the lateral line system. Philos Trans R Soc Lond B 349:119–134
Will U (1982) Efferent neurons of the lateral-line system and the VIII cranial nerve in the brainstem of anurans. Cell Tissue Res 225:673–685
Will U, Fritzsch B (1988) The eighth nerve of amphibians. Peripheral and central distribution. In: Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, Walkowiak W (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 159–183
Yamada Y (1973) Fine structure of the ordinary lateral line organ. I. The neuromast of lamprey Entosphenus japonicus. J Ultrastruct Res 43:1–17
Yamada Y, Hama K (1972) Fine structure of the lateral-line organ of the common eel, Anguilla japonica. Z Zellforsch 124:454–464
Zidanic M (2002) Cholinergic innervation of the chick basilar papilla. J Comp Neurol 445:159–175
Zidanic M, Fuchs PA (1996) Synapsin-like immunoreactivity in the chick cochlea: specific labeling of efferent terminals. Audit Neurosci 2:347–362
Zottoli SJ, van Horne C (1983) Posterior lateral line afferent and efferent pathways withing the central nervous system the goldfish with special reference to the Mauthner cell. J Comp Neurol 219:100–111
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Köppl, C. (2011). Evolution of the Octavolateral Efferent System. In: Ryugo, D., Fay, R. (eds) Auditory and Vestibular Efferents. Springer Handbook of Auditory Research, vol 38. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7070-1_8
Download citation
DOI: https://doi.org/10.1007/978-1-4419-7070-1_8
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4419-7069-5
Online ISBN: 978-1-4419-7070-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)